Attacks on neonates by a male mangabey (Cercocebus atys)

Aggressive behavior by an adult male toward selected infants and their mothers was observed during a long-term study of reproduction in a captive social group of sooty mangabeys (Cercocebus atys). The highest-ranking adult male in this group was observed to attack and bite three neonates out of a total of 13 infants born in 1982. All three attacks were directed attacks in which infants were grabbed from their mothers and bitten in the head. The first infant was fatally injured; the other two probably would have sustained fatal wounds had the male's canines not been blunted beforehand and had observers not intervened. The attacks were preceded by a pattern in which the male persistently stalked or chased the mother-infant pairs, a behavior first observed in the hours immediately following parturition. Unlike attacks in wild baboon groups following male immigration, these attacks on infants occurred in a stable social group in which the male attacker had been a lifelong resident. This male, however, had gained alpha rank only 3 months before attacking the first infant. These attacks, in the context of other evidence of aggression and wounding, are discussed relative to current models of infanticide in primates.     

Ruptured mycotic aortic aneurysm in a sooty mangabey (Cercocebus atys)

Mycotic aortic aneurysm is a local, irreversible dilatation of the aorta associated with destruction of the vessel wall by infection and is a grave clinical condition associated with high morbidity and mortality in humans. Rupture of aortic aneurysms can be spontaneous, idiopathic, or due to severe trauma, and the condition has been associated with bacterial and, rarely, fungal infections in humans and animals. Here, we describe a case of ruptured spontaneous aortic aneurysm associated with zygomycetic infection in a 21-y-old female sooty mangabey. The animal did not present with any significant clinical signs before being found dead. At necropsy, she was in good body condition, and the thoracic cavity had a large amount of clotted blood filling the left pleural space and surrounding the lung lobes. Near the aortic arch, the descending thoracic aorta was focally perforated (diameter, approximately 0.15 cm), and clotted blood adhered to the tunica adventitia. The aortic intima had multiple, firm, pale-yellow nodules (diameter, 0.25 to 0.5 cm). Histopathologically, these nodules consisted of severe multifocal pyogranulomatous inflammation intermixed with necrosis, fibrin, and broad, infrequently septate, thin-walled fungal hyphae. Immunohistochemistry revealed fungal hyphae characteristic of Mucormycetes (formerly Zygomycetes), and PCR analysis identified the organism as Basidiobolus spp. Dissemination of the fungus beyond the aorta was not noted. Spontaneous aortic aneurysms have been described in nonhuman primates, but this is the first reported case of a ruptured spontaneous aortic aneurysm associated with entomophthoromycetic infection in a sooty mangabey.     

A study of facial growth in the sooty mangabey Cercocebus atys

This study examines the pattern of facial bone growth remodelling in the sooty mangabey (Cercocebus atys) by scanning electron microscopy (SEM) of high-accuracy replicas. The efficacy of the technique is appraised by SEM interpretations of facial remodelling in the crab-eating macaque (Macaca fascicularis) and correlative histological examination. The results indicate that the distribution of depository and resorptive areas in Cercocebus closely parallels that which has been observed in Macaca. It is suggested that the different adult facial morphologies in the sooty mangabey and crab-eating macaque are the result of changes in the rates of remodelling events that may be coupled with different patterns of sutural growth (which could not be studied by SEM).     

A brief report on the social behavior of the crested mangabey (Cercocebus galeritus galeritus) with a comparison to the sooty mangabey (C. torquatus atys)

A group of 38 free ranging crested mangabeys in the Tana River Primate Reserve was studied over a 6-week period for a total of 209.5 hr and behavioral comparisons made to a captive group of sooty mangabeys. Although quantitative comparisons between these two mangabey species are not possible, the present data suggest that these geographically separated mangabeys share several behavioral similarities. Copulatory behavior in both species involved a pattern of female darting and female vocalizing following the mount by the male. Several similarities in agonistic behavior also existed: 1) The victim often returned or stayed within 1 m of the aggressor following an agonistic episode; 2) retaliation in which the victim first fled or avoided the aggressor, then subsequently, chased or lunged at the aggressor, typically while screaming; and 3) frequent redirection of aggression by the victim following an agonistic episode. A dominance rank reversal occurred between the two adult male crested mangabeys with no severe wounding. The rank reversal seemed to be related to two subsequent behaviors which included infant carriage by the deposed alpha in the presence of the new alpha male and female demonstrations of extreme protectiveness of their infants in the presence of the new alpha male. Both of these behaviors have been reported in the sooty mangabey group.     

Developmental patterns of serum luteinizing hormone, gonadal and adrenal steroids in the sooty mangabey (Cercocebus atys)

Serum levels of luteinizing hormone (LH), testosterone, dehydroepiandrosterone sulfate (DHAS), androstenedione and cortisol were determined in multiple samples from 86 sooty mangabeys of varying ages (0-17 years). Testosterone, androstenedione, DHAS and cortisol were measured by radioimmunoassay; LH was determined by in vitro bioassay. Serum LH concentrations were elevated in neonates (less than 6 months) and in animals older than 72 months of age. The higher LH levels were associated with increased circulating concentrations of testosterone in males but not females. The pubertal rise in serum testosterone at approximately 55-60 months of age in males was coincident with rapid body growth. No pubertal growth spurt was observed in females. Serum levels of androstenedione and DHAS were highest during early postnatal life (less than 6 months) with androstenedione exceeding 600 ng/dl in males and 250 micrograms/dl in females, but declined rapidly in both sexes to a baseline of 150 ng/dl by 19 months of age. Serum androstenedione did not fluctuate significantly in adult animals. The pattern of age-related changes in serum DHAS paralleled those of serum androstenedione, whereas serum cortisol values did not change significantly with age. Developmental changes in serum LH, testosterone and body weight suggest that the sooty mangabey matures substantially later than the rhesus monkey. The pattern of serum gonadal and adrenal steroids during sexual maturation is similar to that seen in the baboon with no evidence of an adrenarche.     

Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cercocebus torquatus atys)

Three studies were conducted with female sooty mangabeys to describe the occurrence of perineal swelling during pregnancy and to document the associated patterns of ovarian hormone secretion and sexual behavior. Menstrual cycles and pregnancies were charted in 29 female subjects by recording daily vaginal bleeding and perineal swelling. As in other swelling species, maximum perineal tumescence corresponded with the periovulatory phase of the cycle; however, a second tumescence was recorded during pregnancy, with a peak at 49 days postconception. The swelling patterns were similar with the exception that deturgescence was slower during pregnancy. In a second study, blood samples were obtained weekly from nine females to document the estradiol (E₂) and progesterone (P₄) profiles during pregnancy. Analyses revealed increased E₂ concentrations and low P₄ levels in association with the postconception swelling. A third study compared sexual behavior during ovulatory and post-conception tumescent peaks. Behavioral data revealed that, although there was no overall difference in male mount rate to females during the ovulatory and postconception maximum swelling period, when only the alpha male was considered, significantly fewer mounts were directed to females exhibiting a post-conception versus an ovulatory maximum tumescence.     

Hematology and serum chemistry in the white-crowned mangabey (Cercocebus torquatus lunulatus) and in the mandrill (Mandrillus sphinx)

Abstract: Reference values of some hematologic and plasma chemical parameters were established in two species of clinically normal Cercopithecidae. The following variables were studied in seven mandrills (Mandrillus sphinx) and nine white-crowned mangabeys (Cercocebus torquatus lunulatus): hematocrit, hemoglobin concentration, erythrocyte and leucocyte counts, mean corpuscular volume, mean corpuscular hemoglobin, mean corpuscular hemoglobin concentration, glucose, urea, uric acid, cholesterol, creatinine, aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, creatinine phosphokinase, lactic dehydrogenase, gamma glutamyl transpeptidase, total serum proteins, albumin, globulins, albumin-globulin ratio, sodium, potassium, calcium, magnesium, total phosphorus, chloride, and serum osmolality. Few differences were observed when compared with human hematological data and with other species of Cercopithecidae Primates.     

Glycosylation of the envelope glycoprotein gp130 of simian immunodeficiency virus from sooty mangabey (Cercocebus atys).

The envelope glycoprotein 130 ('130' referring to an Mr of 130,000) of simian immunodeficiency virus from sooty mangabey (Cercocebus atys) (SIVSM) was isolated from the cell-free supernatant of the SIVSM-infected human T-cell line H9, metabolically labelled with D-[6-3H]glucosamine. After digestion with Staphylococcus aureus V8 proteinase, radiolabelled N-glycans were liberated from resulting glycopeptides by sequential treatment with endo-beta-N-acetylglucosaminidase H and peptide:N-glycosidase F and fractionated by h.p.l.c. and gel filtration. Individual oligosaccharide species were characterized by enzymic microsequencing, chromatographic analyses and, in part, by acetolysis. The oligosaccharide structures thus established include oligomannosidic glycans with five to nine mannose residues as well as fucosylated and partially sialylated bi-, tri- and tetra-antennary N-acetyl-lactosaminic oligosaccharide species, the latter of which carry, in part, additional galactose residues or N-acetyl-lactosamine repeats. In comparison with the corresponding envelope glycoprotein 120 from human immunodeficiency virus type 1 (HIV-1), propagated in the same cell line [Geyer, Holschbach, Hunsmann and Schneider (1988) J. Biol. Chem. 263, 11760-11767], carbohydrates of the simian glycoprotein were found to consist of decreased amounts of oligomannosidic glycans and increased quantities of higher-branched N-acetyl-lactosaminic species.     

Isolation and characterization of the first simian immunodeficiency virus from a feral sooty mangabey (Cercocebus atys) in West Africa

Abstract: The lineage of HIV-2-like viruses was studied in feral sooty mangabeys (SMs) by serological and genetic methods. Four feral sooty mangabeys were positive for simian immunodeficiency virus (SIV) antibodies and a new isolate, SIV_smSL92a, was obtained. Genetic analysis of gag genes showed that SIV_smSL92a was highly diverse and a distinct sequence subtype within the SIV_sm/HIV-2 family. The results showed that SIV_sm is the most diverse group of SIVs found thus far in a single monkey species.     

Infant carrying by adult male mangabeys (Cercocebus atys)

Sixty-five interactions where an adult male carried an infant in the proximity of a second male were observed during a 19-mo period in a captive sooty mangabey (Cercocebus atys) social group. The behavior was distributed nonrandomly in both the adult male and infant classes. In all but three of the interactions, the recently deposed alpha male carried an infant in the presence of the newly ascendant dominant male. In the first phase of the study, infants that were carried included the entire unweaned infant cohort (n = 5) born before the rank reversal. The rate of carrying in this class declined as a function of increasing infant age and time since the rank reversal. Infant carrying was not observed in the context of fighting, which was rare, and intermale aggression never preceded the behavior. However, in 40% of the cases, carrying occurred after an infant had been threatened by the dominant male. These results suggest that infant carrying served to protect the infant from aggression rather than to exploit the infant as an agonistic buffer. The data did not unequivocally support the postulate that carrying may be a form of paternal care since paternity could not be assessed. The similar structural and contextual patterns of infant carrying in this species suggest a common origin for triadic male-infant interactions in mangabeys and baboons.     

Validation of radioimmunoassays for LH and FSH in the sooty mangabey (Cercocebus atys): Characterization of LH and the response to GnRH

Heterologous radioimmunoassays (RIA) for macaque LH and FSH were validated for the measurement of these hormones in the sooty mangabey and mangabey pituitary LH was characterized relative to rhesus monkey LH. Dilutions of a pituitary mangabey extract and a partially purified preparation of mangabey LH ran parallel to a rhesus monkey standard (LER 1909-2) in the ovine-ovine (o-o) LH assay but showed some deviation from parallelism in the rhesus monkey FSH assay. The LH potency of the mangabey extract and standard were six and 190 times more potent, respectively, than LER 1909-2 in the LH RIA. Mangabey LH was estimated to have a molecular weight of 40,000–42,000 daltons vs 35,000–38,000 daltons for rhesus LH on Sephadex G-100 chromatography. Plasma levels of radioimmunoreactive LH, FSH, and testosterone were assayed before and after a bolus administration of 25, 50, or 100 μg synthetic go-nadotropin releasing hormone (GnRH) to adult male mangabeys. A significant increase in serum levels of LH was seen within 30 min with levels more than fourfold higher than the basal level of LH after administration of 100 μg GnRH. However, no consistent increases in plasma FSH values were detected. The integrated mean LH response above preinjection levels following 25, 50, or 100 μg GnRH was dose related. Serum levels of testosterone were also elevated after administration of GnRH, but peak concentrations of testosterone lagged behind peak levels of LH by approximately 30 min. These studies indicate that the heterologous RIAs may be used for measuring gonadotropins in the mangabey and that the male mangabey is apparently more sensitive to GnRH than the rhesus monkey.     

Spontaneous gastric carcinomas in sooty mangabeys (Cercocebus atys)

Sooty mangabeys (Cercocebus atys) are native to West Africa and are a natural host of SIV, which is implicated in the origin of HIV2. They have been used in studies of AIDS pathogenesis, leprosy, immune responses, reproductive biology, and behavior. Spontaneous tumors have rarely been reported in this species. However, we noted spontaneous gastric carcinomas in 8 sooty mangabeys. Four male and 4 female mangabeys had mild to severe chronic weight loss, with abdominal distention in 5 of 8 animals. At necropsy, 7 of the 8 mangabeys had prominent large ulcerated masses with severe, diffuse thickening of the pyloric wall at or near the gastric-duodenal junction, which often partially occluded the gastric lumen. Early carcinoma was an incidental finding in one mangabey. Histologically, all of the tumors were classified as adenocarcinomas. Adenocarcinomas were noncircumscribed with infiltrates of neoplastic epithelial cells, often arranged in acini. In 3 mangabeys, these infiltrates were transmural and invaded surrounding tissue locally. The adenocarcinomas were locally invasive, with metastasis to regional lymph nodes in 2 animals, but widespread metastasis was not seen. Anisocytosis, anisokaryosis, and high mitotic rates were seen in all 8 tumors. In the samples available, serology and Steiner stain did not detect Helicobacter, and immunohistochemistry failed to reveal Helicobacter or Epstein-Barr virus, 2 potential causes for human gastric carcinomas.     

Affiliative behavior of adult female sooty mangabeys (Cercocebus atys)

A 14-month study of 30 adult female members of a captive group of sooty mangabeys investigated their affiliative interactions with group members of varying age and sex. The adult females preferentially affiliated with other adults and interacted less than expected with immature group members. Dyadic frequencies suggested especially frequent affiliation with the three resident adult males, although the pattern of interaction with each male was distinct and apparently was related to age and dominance status of the males. Females of the alpha matriline showed significantly greater affiliation with the males than did those of other matrilines, but this preference was not reciprocated by the males. A preference for grooming older group members (some of the matriarchs and the oldest adult male) was also suggested. In consideration of the taxonomic distinctness of the sooty mangabey from the gray-cheeked mangabey, comparison of these results with those available for albigena were made. Few differences were apparent. Comparisons with the affiliative behavior of Papio females also suggested limited differences, despite the apparently isolated position of the sooty mangabey within the tribe Papionini.     

Ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus)

I investigated the ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus), one of the world's most endangered primates, with the goal of recommending management strategies. I systematically selected 31 forest fragments throughout the mangabey's 60-km distribution along the lower Tana River in southeastern Kenya. Within the 31 fragments, I measured vegetation structure, food abundance, and human forest product use in 107 belt transects, and conducted 370 mangabey surveys. I used a weighted multiple regression analysis to determine whether there was a dependence between the selected forest attributes and the mean number of mangabey groups per fragment. Fragment area and density of trees > or =10 cm diameter at breast height (DBH) were the only variables that significantly correlated with the variation in mangabey abundance. No additional variables were significant when the analysis was limited to forest fragments inside the Tana River Primate National Reserve (TRPNR) or to fragments outside the TRPNR. When I estimated the resources available before recent human forest product use by adding nonharvested and harvested variables, the total basal area of the top 15 food species became significant. This was only within the TRPNR, however. Management, therefore, should focus on increasing forest area, density of trees > or =10 cm DBH, and coverage of food trees throughout the mangabey's distribution. Solutions must be found for the problem of forest clearing, and forest product use must be better managed to protect the habitat of this critically endangered primate. The significance of food abundance only within the TRPNR suggests a need to collect dietary data from mangabey groups in fragments toward the southern limit of the mangabey's distribution, where plant species composition differs from that in fragments in which dietary data have been previously collected.     

Cerebral Amyloid Angiopathy in an Aged Sooty Mangabey (Cercocebus atys)

A 26-y-old male sooty mangabey (Cercocebus atys) was found at necropsy to have a moderate degree of cerebral amyloid β (Aβ) angiopathy in superficial and parenchymal blood vessels of the brain. Senile (Aβ) plaques were absent, as were neurofibrillary tangles and other signs of neurodegeneration. Affected blood vessels were arterial, capillary, and, less frequently, venous in nature. Histologically, the Aβ40 isoform was more prevalent than was Aβ42. As in humans but unlike in squirrel monkeys, the density of lesions in this mangabey increased along a rostral-to-caudal gradient. Therefore mangabeys appear to conform to the general tendency of nonhuman primates by developing cerebral Aβ angiopathy in the absence of other indices of Alzheimer-type neuropathology.Abbreviations: Aβ, amyloid β, CAA, cerebral amyloid angiopathy, GFAP, glial fibrillary acidic protein, Iba 1, microglia-expressed calcium-binding proteinOne of the most common microvasculopathies in the aging human brain is cerebral amyloid angiopathy (CAA), a disorder in which various aggregation-prone proteins accumulate in the walls of parenchymal and meningeal blood vessels.^4,9 Most often, the amyloidogenic protein is amyloid β (Aβ), a cleavage product of the Aβ precursor protein and the essential component of senile plaques in Alzheimer disease.^13,43 In the brain vasculature, the basal lamina is a primary site of Aβ deposition.^25,35 Severely affected arterioles show a loss of smooth muscle cells in the tunica media, a weakening of the vascular wall and a propensity to rupture.^3,34 CAA thus increases the risk of intracerebral bleeding and may be responsible for as much as 20% of nontraumatic hemorrhagic stroke in elderly humans.^15,18,35 CAA is present to various degrees in virtually all cases of Alzheimer disease,^15,16,21 but it also occurs independently.²⁴ As is the case for other proteopathies, advancing age is a significant risk factor for CAA.^8,19In humans, CAA most often affects the arteries and arterioles of the brain, particularly those in the leptomeninges and cortex.^2,25 CAA is less frequent in veins and capillaries,²⁵ but capillary CAA can be prominent in some cases.^26,33 The occipital lobe is affected most often^1,32,37 but all cortical regions are vulnerable. CAA is variable in occurrence in the cerebellum and uncommon in deep telencephalic gray structures, white matter, and the brainstem,³⁶ except in severely affected cases.³²Although its specific role in the pathogenesis of Alzheimer disease remains uncertain, there is now strong evidence that dementia is exacerbated by CAA.¹⁴ Furthermore, CAA is independently linked to cognitive decline both in rare familial cases²⁰ and in older humans with idiopathic CAA.^2,20 Despite the prevalence of cerebrovascular amyloidosis in elderly humans, surprisingly little is known about its effect on the brain, in part because of a paucity of natural animal models that closely mimic the human disorder.^17,38Nonhuman primates offer a unique opportunity to view CAA from a comparative perspective, given that they normally generate human-sequence Aβ and develop severe cerebral Aβ amyloidosis in old age, generally in the absence of other changes that characterize Alzheimer disease.¹² Nonhuman primates have the additional advantage that, compared with humans, their relatively small brains enable exhaustive regional analysis of microscopic lesions, something that, for practical reasons, is seldom undertaken in the human brain. Here we present the first investigation of age-associated brain changes in sooty mangabeys, focusing in particular on Aβ deposition and related abnormalities. One of the 2 aged mangabeys analyzed had Aβ deposition in the brain which was almost exclusively in the form of CAA. Remarkably, the vessel types affected and the regional distribution of CAA more closely resembled the pattern seen in humans than that in other nonhuman primates, particularly squirrel monkeys.⁶ Differences and similarities in CAA among primate species could provide fresh insights into the development of cerebral amyloidosis and related disorders in older humans.